Viability and expression of sexual ornaments in the barn swallow Hirundo rustica: a meta-analysis.

Sexual selection results in the evolution of exaggerated secondary sexual characters that can entail a viability cost. However, in species where sexual ornaments honestly reflect individual quality, the viability cost of secondary sexual characters may be overwhelmed by variation in individual quality, leading to expect that individuals with the largest secondary sexual characters show higher, rather than lower viability. Here, we used meta-analyses to test whether such expected positive relationship between sexual ornamentation and viability exists in the barn swallow Hirundo rustica, which is one of the most studied model species of sexual selection under field conditions. We found a mean positive effect size of viability in relation to the expression of secondary sexual characters of 0.181 (CI: 0.084-0.278), indicating that in this species the more ornamented individuals are more viable, and therefore of high quality. Analyses of moderator variables showed similar effects in males and females, the H. r. rustica subspecies rather than others and tail length rather than other secondary sexual characters. Future research emphasis on other subspecies than the European one and secondary sexual characters than tail length may help identify the sources of heterogeneity in effect sizes.

Morphological constraints on changing avian migration phenology.

Many organisms at northern latitudes have responded to climate warming by advancing their spring phenology. Birds are known to show earlier timing of spring migration and reproduction in response to warmer springs. However, species show heterogeneous phenological responses to climate warming, with those that have not advanced or have delayed migration phenology experiencing population declines. Although some traits (such as migration distance) partly explain heterogeneity in phenological responses, the factors affecting interspecies differences in the responsiveness to climate warming have yet to be fully explored. In this comparative study, we investigate whether variation in wing aspect ratio (reflecting relative wing narrowness), an ecomorphological trait that is strongly associated with flight efficiency and migratory behaviour, affects the ability to advance timing of spring migration during 1960-2006 in a set of 80 European migratory bird species. Species with larger aspect ratio (longer and narrower wings) showed smaller advancement of timing of spring migration compared to species with smaller aspect ratio (shorter and wider wings) while controlling for phylogeny, migration distance and other life-history traits. In turn, migration distance positively predicted aspect ratio across species. Hence, species that are better adapted to migration appear to be more constrained in responding phenologically to rapid climate warming by advancing timing of spring migration. Our findings corroborate the idea that aspect ratio is a major evolutionary correlate of migration, and suggest that selection for energetically efficient flights, as reflected by high aspect ratio, may hinder phenotypically plastic/microevolutionary adjustments of migration phenology to ongoing climatic changes.

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica).

Parents should differentially invest in sons or daughters depending on the sex-specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin-based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce 'sexy sons' and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.

Faecal egg counts from field experiment reveal density dependence in helminth fecundity: Strongyloides robustus infecting grey squirrels (Sciurus carolinensis).

Investigation of endo-macroparasite infections in living animals relies mostly on indirect methods aimed to detect parasite eggs in hosts' faeces. However, faecal flotation does not provide quantitative information on parasite loads, whereas faecal egg count (FEC) techniques may not give reliable estimates of parasite intensity, since egg production may be affected by density-dependent effects on helminth fecundity. We addressed this issue using Eastern grey squirrels (Sciurus carolinensis) and their gastrointestinal nematode Strongyloides robustus to assess the performance of coprological techniques and to investigate factors affecting parasite fecundity. We compared results of gut examination, flotation and McMaster FECs in 65 culled grey squirrels. Sensitivity and specificity of flotation were 81.2% (Confidence Interval, CI 54.3-95.9%) and 85.7% (CI 72.7-94.1%), respectively, resulting in low positive predictive values when infection prevalence is low. Individual parasite fecundity (no. of eggs/adult female worm) was negatively affected by S. robustus intensity, leading to a non-linear relationship between parasite load and eggs/gram of faeces (EPG). As a consequence, whereas flotation may be a valid method to perform the first screening of infection status, FECs are not a reliable method to estimate S. robustus intensity, since diverse values of EPG may correspond to the same number of parasites. Neither the amount of analysed faeces nor the season had any effect on EPG, indicating that the observed reduction in helminth fecundity is likely caused exclusively by density-dependent processes such as competition among worms or host immune response.

With a little help from my kin: barn swallow nestlings modulate solicitation of parental care according to nestmates' need.

In altricial species, offspring competing for access to limiting parental resources (e.g. food) are selected to achieve an optimal balance between the costs of scrambling for food, the benefits of being fed and the indirect costs of subtracting food to relatives. As the marginal benefits of acquiring additional food decrease with decreasing levels of need, satiated offspring should be prone to favour access to food by their needy kin, thus enhancing their own indirect fitness, while concomitantly reducing costs of harsh competition with hungry broodmates. We tested this prediction in feeding trials of barn swallow (Hirundo rustica) nestlings by comparing begging behaviour and food intake of two similar-sized nestmates, one of which was food-deprived (FD). Non-food-deprived (NFD) offspring modulated begging intensity depending on their nestmate's need: when competing with FD nestmates, NFD nestlings reduced both the intensity and frequency of begging displays compared to themselves in the control trial before food deprivation. Hence, NFD nestlings reduced their competitiveness to the advantage of FD nestmates, which obtained more feedings and showed a threefold larger increase in body mass. Moderation of individual selfishness can therefore be adaptive in the presence of a needier kin, because the indirect fitness benefits of promoting its condition can outweigh the costs of forgoing being fed, and because it limits the cost of begging escalation against a vigorous competitor.

MHC genotype predicts mate choice in the ring-necked pheasant Phasianus colchicus.

Females of several vertebrate species selectively mate with males on the basis of the major histocompatibility complex (MHC) genes. As androgen-mediated maternal effects have long-lasting consequences for the adult phenotype, both mating and reproductive success may depend on the combined effect of MHC genotype and exposure to androgens during early ontogeny. We studied how MHC-based mate choice in ring-necked pheasants (Phasianus colchicus) was influenced by an experimental in ovo testosterone (T) increase. There was no conclusive evidence of in ovo T treatment differentially affecting mate choice in relation to MHC genotype. However, females avoided mating with males with a wholly different MHC genotype compared with males sharing at least one MHC allele. Females also tended to avoid mating with MHC-identical males, though not significantly so. These findings suggest that female pheasants preferred males with intermediate MHC dissimilarity. Male MHC heterozygosity or diversity did not predict the expression of ornaments or male dominance rank. Thus, MHC-based mating preferences in the ring-necked pheasant do not seem to be mediated by ornaments' expression and may have evolved mainly to reduce the costs of high heterozygosity at MHC loci for the progeny, such as increased risk of autoimmune diseases or disruption of coadapted gene pools.

Rapid change in host use of the common cuckoo Cuculus canorus linked to climate change.

Parasites require synchrony with their hosts so if host timing changes with climate change, some parasites may decline and eventually go extinct. Residents and short-distance migrant hosts of the brood parasitic common cuckoo, Cuculus canorus, have advanced their phenology in response to climate change more than long-distance migrants, including the cuckoo itself. Because different parts of Europe show different degrees of climate change, we predicted that use of residents or short-distance migrants as hosts should have declined in areas with greater increase in spring temperature. Comparing relative frequency of parasitism of the two host categories in 23 European countries before and after 1990, when spring temperatures in many areas had started to increase, we found that relative parasitism of residents and short-distance migrants decreased. This change in host use was positively related to increase in spring temperature, consistent with the prediction that relative change in phenology for different migrant classes drives host-use patterns. These findings are consistent with the hypothesis that climate change affects the relative abundance of different host races of the common cuckoo.

Sex-related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry.

Timing of arrival/emergence to the breeding grounds is under contrasting natural and sexual selection pressures. Because of differences in sex roles and physiology, the balance between these pressures on either sex may differ, leading to earlier male (protandry) or female (protogyny) arrival. We test several competing hypotheses for the evolution of protandry using migration data for 22 bird species, including for the first time several monochromatic ones where sexual selection is supposedly less intense. Across species, protandry positively covaried with sexual size dimorphism but not with dichromatism. Within species, there was weak evidence that males migrate earlier because, being larger, they are less susceptible to adverse conditions. Our results do not support the 'rank advantage' and the 'differential susceptibility' hypotheses, nor the 'mate opportunity' hypothesis, which predicts covariation of protandry with dichromatism. Conversely, they are compatible with 'mate choice' arguments, whereby females use condition-dependent arrival date to assess mate quality.

Maternal allocation strategies and differential effects of yolk carotenoids on the phenotype and viability of yellow-legged gull (Larus michahellis) chicks in relation to sex and laying order.

Egg quality may mediate maternal allocation strategies according to progeny sex. In vertebrates, carotenoids have important physiological roles during embryonic and post-natal life, but the consequences of variation in yolk carotenoids for offspring phenotype in oviparous species are largely unknown. In yellow-legged gulls, yolk carotenoids did not vary with embryo sex in combination with egg laying date, order and mass. Yolk lutein supplementation enhanced the growth of sons from first eggs but depressed that of sons from last eggs, enhanced survival of daughters late in the season, and promoted immunity of male chicks and chicks from small eggs. Lack of variation in egg carotenoids in relation to sex and egg features, and the contrasting effects of lutein on sons and daughters, do not support the hypothesis of optimal sex-related egg carotenoid allocation. Carotenoids transferred to the eggs may rather result from a trade-off between opposing effects on sons or daughters.

Barn swallow chicks beg more loudly when broodmates are unrelated.

Parents of a variety of animal species distribute critical resources among their offspring according to the intensity of begging displays. Kin selection theory predicts that offspring behave more selfishly in monopolizing parental care as relatedness with competitors declines. We cross-fostered two eggs between barn swallow (Hirundo rustica) clutches and compared the loudness of begging between mixed and control broods under normal feeding conditions and after a period of food deprivation. Begging loudness was higher in mixed broods under normal but not poor feeding conditions. Survival was reduced in mixed than control broods. Call features varied according to parentage, possibly serving as a cue for self-referent phenotype matching in mixed broods. This is the first evidence within a vertebrate species that competitive behaviour among broodmates depends on their relatedness. Thus, kin recognition and relatedness may be important determinants of communication among family members, care allocation and offspring viability in barn swallows.

Interspecific variation in egg testosterone levels: implications for the evolution of bird song.

Although interspecific variation in maternal effects via testosterone levels can be mediated by natural selection, little is known about the evolutionary consequences of egg testosterone for sexual selection. However, two nonexclusive evolutionary hypotheses predict an interspecific relationship between egg testosterone levels and the elaboration of sexual traits. First, maternal investment may be particularly enhanced in sexually selected species, which should generate a positive relationship. Secondly, high prenatal testosterone levels may constrain the development of sexual characters, which should result in a negative relationship. Here we investigated these hypotheses by exploring the relationship between yolk testosterone levels and features of song in a phylogenetic study of 36 passerine species. We found that song duration and syllable repertoire size were significantly negatively related to testosterone levels in the egg, even if potentially confounding factors were held constant. These relationships imply that high testosterone levels during early development of songs may be detrimental, thus supporting the developmental constraints hypothesis. By contrast, we found significant evidence that song-post exposure relative to the height of the vegetation is positively related to egg testosterone levels. These results support the hypothesis that high levels of maternal testosterone have evolved in species with intense sexual selection acting on the location of song-posts. We found nonsignificant effects for intersong interval and song type repertoire size, which may suggest that none of the above hypothesis apply to these traits, or they act simultaneously and have opposing effects.

Elevated frequency of abnormalities in barn swallows from Chernobyl.

Ever since the Chernobyl accident in 1986, that contaminated vast areas in surrounding countries with radiation, abnormalities and birth defects have been reported in human populations. Recently, several studies suggested that the elevated frequency of such abnormalities can be attributed to poverty and stress in affected human populations. Here, we present long-term results for a free-living population of barn swallows, Hirundo rustica, demonstrating the presence of 11 morphological abnormalities in populations around Chernobyl, but much less frequently in an uncontaminated Ukrainian control population and three more distant control populations. The presence of these abnormalities in barn swallows is associated with reduced viability. These findings demonstrate a link between morphological abnormalities and radiation in an animal population that cannot be attributed to poverty and stress. The most parsimonious hypothesis for abnormalities in animal and human populations alike is that the effects are caused by the same underlying cause, viz. radiation derived from the Chernobyl accident.

Maternal effects and the evolution of brain size in birds: overlooked developmental constraints.

A central dogma for the evolution of brain size posits that the maintenance of large brains incurs developmental costs, because they need prolonged periods to grow during the early ontogeny. Such constraints are supported by the interspecific relationship between ontological differences and relative brain size in birds and mammals. Given that mothers can strongly influence the development of the offspring via maternal effects that potentially involve substances essential for growing brains, we argue that such effects may represent an important but overlooked component of developmental constraints on brain size. To demonstrate the importance of maternal effect on the evolution of brains, we investigated the interspecific relationship between relative brain size and maternal effects, as reflected by yolk testosterone, carotenoids, and vitamins A and E in a phylogenetic study of birds. Females of species with relatively large brains invested more in eggs in terms of testosterone and vitamin E than females of species with small brains. The effects of carotenoid and vitamin A levels on the evolution of relative brain size were weaker and non-significant. The association between relative brain size and yolk testosterone was curvilinear, suggesting that very high testosterone levels can be suppressive. However, at least in moderate physiological ranges, the positive relationship between components of maternal effects and relative brain size may imply one aspect of developmental costs of large brains. The relationship between vitamin E and relative brain size was weakened when we controlled for developmental mode, and thus the effect of this antioxidant may be indirect. Testosterone-enhanced neurogenesis and vitamin E-mediated defence against oxidative stress may have key functions when the brain of the embryo develops, with evolutionary consequences for relative brain size.

Increased egg estradiol concentration feminizes digit ratios of male pheasants (Phasianus colchicus).

The length ratio between individual digits differs between males and females in humans, other mammals, lizards, and one bird species. Sexual dimorphism in digit ratios and variation among individuals of the same sex may depend on differential exposure to androgens and estrogens during embryonic life. Organizational effects of sex hormones could cause the observed correlations between digit ratios and diverse phenotypic traits in humans. However, no study has investigated experimentally the effect of prenatal estrogens on digit ratios. We analyzed the effect of estradiol injection in ring-necked pheasant (Phasianus colchicus) eggs on digit ratios. Males from control eggs had higher ratios between the second or third and the fourth digit of the right foot compared to females. Estradiol-treated eggs produced males with lower (feminized) right foot second to fourth digit ratio. Thus, we provided the first experimental evidence that prenatal exposure to physiologically high estrogen levels affects bird digit ratios.

Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks.

Maternal effects mediated by egg quality are important sources of offspring phenotypic variation and can influence the course of evolutionary processes. Mothers allocate to the eggs diverse antioxidants that protect the embryo from oxidative stress. In the yellow-legged gull (Larus michahellis), yolk antioxidant capacity varied markedly among clutches and declined considerably with egg laying date. Analysis of bioptic yolk samples from clutches that were subsequently partially cross-fostered revealed a positive effect of yolk antioxidant capacity on embryonic development and chick growth, but not on immunity and begging behaviour, while controlling for parentage and common environment effects. Chick plasma antioxidant capacity varied according to rearing environment, after statistically partitioning out maternal influences mediated by egg quality. Thus, the results of this study indicate that egg antioxidants are important mediators of maternal effects also in wild bird populations, especially during the critical early post-hatching phase.

An analysis of continent-wide patterns of sexual selection in a passerine bird.

Patterns of selection are widely believed to differ geographically, causing adaptation to local environmental conditions. However, few studies have investigated patterns of phenotypic selection across large spatial scales. We quantified the intensity of selection on morphology in a monogamous passerine bird, the barn swallow Hirundo rustica, using 6495 adults from 22 populations distributed across Europe and North Africa. According to the classical Darwin-Fisher mechanism of sexual selection in monogamous species, two important components of fitness due to sexual selection are the advantages that the most attractive males acquire by starting to breed early and their high annual fecundity. We estimated directional selection differentials on tail length (a secondary sexual character) and directional selection gradients after controlling for correlated selection on wing length and tarsus length with respect to these two fitness components. Phenotype and fitness components differed significantly among populations for which estimates were available for more than a single year. Likewise, selection differentials and selection gradients differed significantly among populations for tail length, but not for the other two characters. Sexual selection differentials differed significantly from zero across populations for tail length, particularly in males. Controlling statistically for the effects of age reduced the intensity of selection by 60 to 81%, although corrected and uncorrected estimates were strongly positively correlated. Selection differentials and gradients for tail length were positively correlated between the sexes among populations for selection acting on breeding date, but not for fecundity selection. The intensity of selection with respect to breeding date and fecundity were significantly correlated for tail length across populations. Sexual size dimorphism in tail length was significantly correlated with selection differentials with respect to breeding date for tail length in male barn swallows across populations. These findings suggest that patterns of sexual selection are consistent across large geographical scales, but also that they vary among populations. In addition, geographical patterns of phenotypic selection predict current patterns of phenotypic variation among populations, suggesting that consistent patterns of selection have been present for considerable amounts of time.

Differential effects of egg albumen content on barn swallow nestlings in relation to hatch order.

In diverse animal taxa, egg mass variation mediates maternal effects with long-term consequences for offspring ontogeny and fitness. Patterns of egg mass variation with laying order differ considerably among birds, but no study has experimentally investigated the function of variation in albumen or yolk egg content in the wild. In barn swallows (Hirundo rustica), absolute and relative albumen mass increased with egg laying order. Experimental albumen removal delayed hatching, had larger negative effects on growth of late-hatched nestlings, and reduced nestling survival. Laying order positively predicted hatch order. Because nestling competitive ability depends on size, and albumen egg content influences hatchling size, present results suggest that by increasing albumen content of late eggs mothers reduce hatching asynchrony and enhance growth particularly of late-hatched nestlings. Thus, variation in albumen mass with laying order may function to mitigate the negative phenotypic consequences of hatching late in species that adopt a 'brood-survival' strategy.

Geographic variation in the G matrices of wild populations of the barn swallow.

In this paper, we present an analysis of genetic variation in three wild populations of the barn swallow, Hirundo rustica. We estimated the P, E, and G matrices for six linear morphological measurements and tested for variation among populations using the Flury hierarchical method and the jackknife followed by MANOVA method. Because of nonpositive-definite matrices, we had to employ 'bending' to analyse the G and E matrices with the Flury method. Both statistical methods agree in finding that the P and G matrices are significantly different but comparison between the analysis of the P matrices and pairwise analyses of the P, E, and G matrices suggests caution in interpreting the Flury results concerning differences in matrix structure. The significant variation among the populations in the G matrices appears to be due in large measure to the most geographically distant population.

Genetic variation in infestation with a directly transmitted ectoparasite.

Genetic variation in levels of parasitism of hosts is an underlying assumption of studies of coevolution, but few such estimates are available from the field. We studied genetic variation in the abundance of the chewing louse Hirundoecus malleus on its barn swallow host Hirundo rustica. These parasites are directly transmitted and a test of genetic variation of parasite abundance would thus provide a particularly strong test. The prevalence and the abundance of the chewing lice did not differ significantly between adult male and female hosts. The resemblance in parasite intensity of H. malleus of offspring and their parents was positive and highly significant, and an analysis of extra-pair paternity in the host allowed partitioning of this resemblance between genetic and common environment effects. There was no significant resemblance in parasite intensity between extra-pair offspring and their foster parents, although the resemblance remained for within-pair offspring. This provides evidence for the abundance of directly transmitted parasites having an additive genetic component. We found no evidence of common environment effects as parents did not resemble each other with respect to lice abundance.